, Volume 186, Issue 1, pp 233–245

Mapping QTLs with epistatic effects and QTL × treatment interactions for salt tolerance at seedling stage of wheat

  • Yun-Feng Xu
  • Diao-Guo An
  • Dong-Cheng Liu
  • Ai-Min Zhang
  • Hong-Xing Xu
  • Bin Li


Quantitative trait loci (QTLs) with additive (a), additive × additive (aa) epistatic effects, and their treatmental interactions (at and aat) were studied under salt stress and normal conditions at seedling stage of wheat (Triticum aestivum L.). A set of 182 recombinant inbred lines (RILs) derived from cross Xiaoyan 54 × Jing 411 were used. A total of 29 additive QTLs and 17 epistasis were detected for 12 traits examined, among which eight and seven, respectively, were identified to have QTL × treatment effects. Physiological traits rather than biomass traits were more likely to be involved in QTL × treatment interactions. Ten intervals on chromosomes 1A, 1D, 2A (two), 2D, 3B, 4B, 5A, 5B and 7D showed overlapping QTLs for different traits; some of them represent a single locus affecting different traits and/or the same trait under both treatments. Eleven pairs of QTLs were detected on seemingly homoeologous positions of six chromosome groups of wheat, showing synteny among the A, B and D genomes. Ten pairs were detected in which each pair was contributed by the same parent, indicating a strong genetic plasticity of the QTLs. The results are helpful for understanding the genetic basis of salt tolerance in wheat and provide useful information for genetic improvement of salt tolerance in wheat by marker-assisted selection.


Epistasis QTL × treatment Salt tolerance Quantitative trait locus (QTL) Wheat 



Chlorophyll content (SPAD value)


Marker-assisted selection


Normal water treatment


Quantitative trait locus

Q × E

QTL × environment

Q × T

QTL × treatment




Additive × additive


Additive × treatment


Epistasis × treatment


Root dry weight


Recombinant inbred line


Root K+ concentration


Root K+/Na+ concentration ratio


Root length


Root Na+ concentration


Salt stress treatment


Shoot dry weight


Shoot height


Salt injury index


Shoot K+ concentration


Shoot K+/Na+ concentration ratio


Shoot Na+ concentration


Total dry weight


  1. Cao G, Zhu J, He C, Gao Y, Yan J, Wu P (2001) Impact of epistasis and QTL × environment interaction on the developmental behavior of plant height in rice (Oryza sativa L.). Theor Appl Genet 103(1):153–160. doi:10.1007/s001220100536 CrossRefGoogle Scholar
  2. Chhipa BR, Lal P (1995) Na/K ratios as the basis of salt tolerance in wheat. Aust J Agric Res 46(3):533–539CrossRefGoogle Scholar
  3. Doebley J, Stec A, Gustus C (1995) Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141(1):333–346PubMedGoogle Scholar
  4. Doerge RW (2002) Mapping and analysis of quantitative trait loci in experimental populations. Nat Rev Genet 3(1):43–52PubMedCrossRefGoogle Scholar
  5. Fan CC, Yu XQ, Xing YZ, Xu CG, Luo LJ, Zhang QF (2005) The main effects, epistatic effects and environmental interactions of QTLs on the cooking and eating quality of rice in a doubled-haploid line population. Theor Appl Genet 110(8):1445–1452. doi:10.1007/s00122-005-1975-y PubMedCrossRefGoogle Scholar
  6. Foolad MR (1999) Comparison of salt tolerance during seed germination and vegetative growth in tomato by QTL mapping. Genome 42(4):727–734CrossRefGoogle Scholar
  7. Foolad MR, Chen FQ (1999) RFLP mapping of QTLs conferring salt tolerance during the vegetative stage in tomato. Theor Appl Genet 99(1–2):235–243CrossRefGoogle Scholar
  8. Foolad MR, Zhang LP, Lin GY (2001) Identification and validation of QTLs for salt tolerance during vegetative growth in tomato by selective genotyping. Genome 44(3):444–454PubMedCrossRefGoogle Scholar
  9. Genc Y, Oldach K, Verbyla AP, Lott G, Hassan M, Tester M, Wallwork H, McDonald GK (2010) Sodium exclusion QTL associated with improved seedling growth in bread wheat under salinity stress. Theor Appl Genet 121(5):877–894. doi:10.1007/s00122-010-1357-y PubMedCrossRefGoogle Scholar
  10. Gong JM, He P, Qian QA, Shen LS, Zhu LH, Chen SY (1999) Identification of salt-tolerance QTL in rice (Oryza sativa L.). Chin Sci Bull 44(1):68–71CrossRefGoogle Scholar
  11. Groos C, Robert N, Bervas E, Charmet G (2003) Genetic analysis of grain protein-content, grain yield and thousand-kernel weight in bread wheat. Theor Appl Genet 106(6):1032–1040. doi:10.1007/s00122-002-1111-1 PubMedGoogle Scholar
  12. Gupta PK, Mir RR, Mohan A, Kumar J (2008) Wheat genomics: present status and future prospects. Int J Plant Genomics 2008(Article ID 896451):1–36. doi:10.1155/2008/896451 Google Scholar
  13. Han YP, Teng WL, Sun DS, Du YP, Qiu LJ, Xu XL, Li WB (2008) Impact of epistasis and QTL × environment interaction on the accumulation of seed mass of soybean (Glycine max L. Merr.). Genet Res 90(6):481–491. doi:10.1017/S0016672308009865 CrossRefGoogle Scholar
  14. Hoagland D, Arnon D (1950) The water culture method for growing plants without soil. California Agricultural Experiment Station Circular: 347Google Scholar
  15. Jansen RC, Vanooijen JW, Stam P, Lister C, Dean C (1995) Genotype-by-environment interaction in genetic mapping of multiple quantitative trait loci. Theor Appl Genet 91(1):33–37CrossRefGoogle Scholar
  16. Jiang CJ, Zeng ZB (1995) Multiple trait analysis of genetic mapping for quantitative trait loci. Genetics 140(3):1111–1127PubMedGoogle Scholar
  17. Kumar N, Kulwal PL, Balyan HS, Gupta PK (2007) QTL mapping for yield and yield contributing traits in two mapping populations of bread wheat. Mol Breeding 19(2):163–177. doi:10.1007/s11032-006-9056-8 CrossRefGoogle Scholar
  18. Lee SY, Ahn JH, Cha YS, Yun DW, Lee MC, Ko JC, Lee KS, Eun MY (2006) Mapping of quantitative trait loci for salt tolerance at the seedling stage in rice. Mol Cells 21(2):192–196PubMedGoogle Scholar
  19. Li SS, Jia JZ, Wei XY, Zhang XC, Li LZ, Chen HM, Fan YD, Sun HY, Zhao XH, Lei TD, Xu YF, Jiang FS, Wang HG, Li LH (2007) A intervarietal genetic map and QTL analysis for yield traits in wheat. Mol Breeding 20(2):167–178CrossRefGoogle Scholar
  20. Li ZS, Li B, Tong YP (2008) The contribution of distant hybridization with decaploid Agropyron elongatum to wheat improvement in China. J Genet Genomics 35(8):451–456PubMedCrossRefGoogle Scholar
  21. Liao CY, Wu P, Hu B, Yi KK (2001) Effects of genetic background and environment on QTLs and epistasis for rice (Oryza sativa L.) panicle number. Theor Appl Genet 103(1):104–111CrossRefGoogle Scholar
  22. Lin HX, Zhu MZ, Yano M, Gao JP, Liang ZW, Su WA, Hu XH, Ren ZH, Chao DY (2004) QTLs for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance. Theor Appl Genet 108(2):253–260. doi:10.1007/s00122-003-1421-y PubMedCrossRefGoogle Scholar
  23. Lindsay MP, Lagudah ES, Hare RA, Munns R (2004) A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Funct Plant Biol 31(11):1105–1114. doi:10.1071/Fp04111 CrossRefGoogle Scholar
  24. Liu X, Shi J, Zhang XY, Ma YS, Jia JZ (2001) Screening salt tolerance germplasms and tagging the tolerance gene(s) using microsatellite (SSR) markers in wheat. Acta Bot Sin 43(9):948–954Google Scholar
  25. Liu G, Yang J, Xu H, Zhu J (2007) Influence of epistasis and QTL × environment interaction on heading date of rice (Oryza sativa L.). J Genet Genomics 34(7):608–615PubMedCrossRefGoogle Scholar
  26. Ma LQ, Zhou EF, Huo NX, Zhou RH, Wang GY, Jia JZ (2007a) Genetic analysis of salt tolerance in a recombinant inbred population of wheat (Triticum aestivum L.). Euphytica 153(1–2):109–117Google Scholar
  27. Ma XQ, Tang JH, Teng WT, Yan JB, Meng YJ, Li JS (2007b) Epistatic interaction is an important genetic basis of grain yield and its components in maize. Mol Breeding 20(1):41–51. doi:10.1007/s11032-006-9071-9 CrossRefGoogle Scholar
  28. Mano Y, Takeda K (1997) Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley (Hordeum vulgare L.). Euphytica 94(3):263–272CrossRefGoogle Scholar
  29. Marza F, Bai GH, Carver BF, Zhou WC (2006) Quantitative trait loci for yield and related traits in the wheat population Ning7840 × Clark. Theor Appl Genet 112(4):688–698. doi:10.1007/s00122-005-0172-3 PubMedCrossRefGoogle Scholar
  30. Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253(1):201–218CrossRefGoogle Scholar
  31. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi:10.1146/annurev.arplant.59.032607.092911 PubMedCrossRefGoogle Scholar
  32. Pardo JM (2010) Biotechnology of water and salinity stress tolerance. Curr Opin Biotechnol 21(2):185–196. doi:10.1016/j.copbio.2010.02.005 PubMedCrossRefGoogle Scholar
  33. Paterson AH (1995) Molecular dissection of quantitative traits: progress and prospects. Genome Res 5(4):321–333PubMedCrossRefGoogle Scholar
  34. Peleg Z, Fahima T, Krugman T, Abbo S, Yakir D, Korol AB, Saranga Y (2009) Genomic dissection of drought resistance in durum wheat × wild emmer wheat recombinant inbreed line population. Plant, Cell Environ 32(7):758–779. doi:10.1111/j.1365-3040.2009.01956.x CrossRefGoogle Scholar
  35. Pitman MG, Läuchli A (2004) Global impact of salinity and agricultural ecosystems. In: Läuchli A, Lüttge U (eds) Salinity: environment-plants-molecules. Kluwer Academic, Dordrecht, pp 3–20CrossRefGoogle Scholar
  36. Prasad SR, Bagali PG, Hittalmani S, Shashidhar HE (2000) Molecular mapping of quantitative trait loci associated with seedling tolerance to salt stress in rice (Oryza sativa L.). Curr Sci India 78(2):162–164Google Scholar
  37. Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive1 Na+-H+ antiporter during salinity stress. Plant Physiol 136(1):2548–2555. doi:10.1104/pp.104.049213 PubMedCrossRefGoogle Scholar
  38. Quarrie SA, Steed A, Calestani C, Semikhodskii A, Lebreton C, Chinoy C, Steele N, Pljevljakusic D, Waterman E, Weyen J, Schondelmaier J, Habash DZ, Farmer P, Saker L, Clarkson DT, Abugalieva A, Yessimbekova M, Turuspekov Y, Abugalieva S, Tuberosa R, Sanguineti MC, Hollington PA, Aragues R, Royo A, Dodig D (2005) A high-density genetic map of hexaploid wheat (Triticum aestivum L.) from the cross Chinese Spring × SQ1 and its use to compare QTLs for grain yield across a range of environments. Theor Appl Genet 110(5):865–880. doi:10.1007/s00122-004-1902-7 PubMedCrossRefGoogle Scholar
  39. Quarrie SA, Quarrie SP, Radosevic R, Rancic D, Kaminska A, Barnes JD, Leverington M, Ceoloni C, Dodig D (2006) Dissecting a wheat QTL for yield present in a range of environments: from the QTL to candidate genes. J Exp Bot 57(11):2627–2637. doi:10.1093/Jxb/Erl026 PubMedCrossRefGoogle Scholar
  40. Quesada V, García-Martínez S, Piqueras P, Ponce MR, Micol JL (2002) Genetic architecture of NaCl tolerance in Arabidopsis. Plant Physiol 130(2):951–963. doi:10.1104/Pp.006536 PubMedCrossRefGoogle Scholar
  41. Rodriguez-Navarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants. J Exp Bot 57(5):1149–1160. doi:10.1093/Jxb/Erj068 PubMedCrossRefGoogle Scholar
  42. Serrano R (1996) Salt tolerance in plants and microorganisms: toxicity targets and defense responses. Int Rev Cytol 165:1–52PubMedCrossRefGoogle Scholar
  43. Shavrukov Y, Langridge P, Tester M (2009) Salinity tolerance and sodium exclusion in genus Triticum. Breeding Sci 59(5):671–678CrossRefGoogle Scholar
  44. Shen XL, Zhang TZ, Guo WZ, Zhu XF, Zhang XY (2006) Mapping fiber and yield QTLs with main, epistatic, and QTL × environment interaction effects in recombinant inbred lines of upland cotton. Crop Sci 46(1):61–66. doi:10.2135/scopsci2005.0056 CrossRefGoogle Scholar
  45. Sun XY, Wu K, Zhao Y, Kong FM, Han GZ, Jiang HM, Huang XJ, Li RJ, Wang HG, Li SS (2009) QTL analysis of kernel shape and weight using recombinant inbred lines in wheat. Euphytica 165(3):615–624. doi:10.1007/s10681-008-9794-2 CrossRefGoogle Scholar
  46. Takehisa H, Shimodate T, Fukuta Y, Ueda T, Yano M, Yamaya T, Kameya T, Sato T (2004) Identification of quantitative trait loci for plant growth of rice in paddy field flooded with salt water. Field Crop Res 89(1):85–95. doi:10.1016/j.fcr.2004.01.026 CrossRefGoogle Scholar
  47. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot (London) 91(5):503–527. doi:10.1093/Aob/Mcg058 CrossRefGoogle Scholar
  48. Tuberosa R, Salvi S (2007) Dissecting QTLs for tolerance to drought and salinity. In: Jenks MA, Hasegawa PM, Jain M (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer, Dordrecht, pp 381–411CrossRefGoogle Scholar
  49. Veldboom LR, Lee M, Woodman WL (1994) Molecular marker-facilitated studies in an elite maize population: I. Linkage analysis and determination of QTL for morphological traits. Theor Appl Genet 88(1):7–16CrossRefGoogle Scholar
  50. Villalta I, Reina-Sanchez A, Bolarin MC, Cuartero J, Belver A, Venema K, Carbonell EA, Asins MJ (2008) Genetic analysis of Na+ and K+ concentrations in leaf and stem as physiological components of salt tolerance in tomato. Theor Appl Genet 116(6):869–880. doi:10.1007/s00122-008-0720-8 PubMedCrossRefGoogle Scholar
  51. Wang BH, Wu YT, Guo WZ, Zhu XF, Huang NT, Zhang TZ (2007) QTL analysis and epistasis effects dissection of fiber qualities in an elite cotton hybrid grown in second generation. Crop Sci 47(4):1384–1392. doi:10.2135/cropsci2006.10.0647 CrossRefGoogle Scholar
  52. Xing YZ, Tan YF, Hua JP, Sun XL, Xu CG, Zhang Q (2002) Characterization of the main effects, epistatic effects and their environmental interactions of QTLs on the genetic basis of yield traits in rice. Theor Appl Genet 105(2–3):248–257. doi:10.1007/s00122-002-0952-y PubMedGoogle Scholar
  53. Xu YB, Crouch JH (2008) Marker-assisted selection in plant breeding: from publications to practice. Crop Sci 48(2):391–407. doi:10.2135/cropsci2007.04.0191 CrossRefGoogle Scholar
  54. Yang DL, Jing RL, Chang XP, Li W (2007a) Identification of quantitative trait loci and environmental interactions for accumulation and remobilization of water-soluble carbohydrates in wheat (Tiiticum aestivum L.) stems. Genetics 176(1):571–584. doi:10.1534/genetics.106.068361 PubMedCrossRefGoogle Scholar
  55. Yang J, Zhu J, Williams RW (2007b) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23(12):1527–1536. doi:10.1093/bioinformatics/btm143 PubMedCrossRefGoogle Scholar
  56. Yang J, Hu CC, Hu H, Yu RD, Xia Z, Ye XZ, Zhu J (2008) QTLNetwork: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24(5):721–723. doi:10.1093/bioinformatics/btm494 PubMedCrossRefGoogle Scholar
  57. Yu SB, Li JX, Tan YF, Gao YJ, Li XH, Zhang QF, Maroof MAS (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 94(17):9226–9231PubMedCrossRefGoogle Scholar
  58. Zhang KP, Tian JC, Zhao L, Wang SS (2008) Mapping QTLs with epistatic effects and QTL × environment interactions for plant height using a doubled haploid population in cultivated wheat. J Genet Genomics 35(2):119–127PubMedCrossRefGoogle Scholar
  59. Zhang KP, Tian JC, Zhao L, Liu B, Chen GF (2009) Detection of quantitative trait loci for heading date based on the doubled haploid progeny of two elite Chinese wheat cultivars. Genetica 135(3):257–265. doi:10.1007/s10709-008-9274-6 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Yun-Feng Xu
    • 1
  • Diao-Guo An
    • 1
  • Dong-Cheng Liu
    • 2
  • Ai-Min Zhang
    • 2
  • Hong-Xing Xu
    • 1
  • Bin Li
    • 2
  1. 1.Key Laboratory of Agricultural Water Resources, Center for Agricultural Resources Research, Institute of Genetics and Developmental BiologyChinese Academy of SciencesShijiazhuangChina
  2. 2.State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingChina

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